Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1996 Jun;16(6):3138–3155. doi: 10.1128/mcb.16.6.3138

A developmentally modulated chromatin structure at the mouse immunoglobulin kappa 3' enhancer.

M C Roque 1, P A Smith 1, V C Blasquez 1
PMCID: PMC231308  PMID: 8649425

Abstract

Transcription of the mouse immunoglobulin kappa gene is controlled by two enhancers: the intronic enhancer (Ei) that occurs between the joining (J kappa) and constant (C kappa) exons and the 3' enhancer (E3') located 8.5 kb downstream of the gene. To understand the role of E3' in the activation of the mouse immunoglobulin kappa gene, we studied its chromatin structure in cultured B-cell lines arrested at various stages of differentiation. We found that 120 bp of the enhancer's transcriptional core becomes DNase I hypersensitive early in B-cell development. Genomic footprinting of pro-B and pre-B cells localized this chromatin alteration to B-cell-specific protections at the region including the direct repeat (DR) and the sequence downstream of the DR (DS), the PU.1-NFEM-5 site, and the core's E-box motif, identifying bound transcription factors prior to kappa gene rearrangement. Early footprints were, however, not detected at downstream sites proposed to play a negative role in transcription. The early chromatin structure persisted through the mature B-cell stage but underwent a dramatic shift in plasma cells, correlating with the loss of guanosine protection within the DR-DS junction and the appearance of novel footprints at a GC-rich motif upstream and the NF-E1 (YY1/delta)-binding site downstream. Gel shift analysis demonstrated that the DR-DS junction is bound by a factor with properties similar to those of BSAP (B-cell-specific activator protein). These results reveal developmental-stage-specific changes in the composition of nuclear factors bound to E3', clarify the role of factors that bind constitutively in vitro, and point to the differentiation of mature B cells to plasma cells as an important transitional point in the function of this enhancer. The observed changes in nuclear factor composition were accompanied by the rearrangement of positioned nucleosomes that flank the core region, suggesting a role for both nuclear factors and chromatin structure in modulating kappa E3' function during B-cell development. The functional implications of the observed chromatin alterations are discussed in the context of recent studies on kappa E3' and the factors that bind to it.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams B., Dörfler P., Aguzzi A., Kozmik Z., Urbánek P., Maurer-Fogy I., Busslinger M. Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis. Genes Dev. 1992 Sep;6(9):1589–1607. doi: 10.1101/gad.6.9.1589. [DOI] [PubMed] [Google Scholar]
  2. Adams C. C., Workman J. L. Nucleosome displacement in transcription. Cell. 1993 Feb 12;72(3):305–308. doi: 10.1016/0092-8674(93)90109-4. [DOI] [PubMed] [Google Scholar]
  3. Alt F. W., Blackwell T. K., Yancopoulos G. D. Development of the primary antibody repertoire. Science. 1987 Nov 20;238(4830):1079–1087. doi: 10.1126/science.3317825. [DOI] [PubMed] [Google Scholar]
  4. Alt F. W., Rosenberg N., Enea V., Siden E., Baltimore D. Multiple immunoglobulin heavy-chain gene transcripts in Abelson murine leukemia virus-transformed lymphoid cell lines. Mol Cell Biol. 1982 Apr;2(4):386–400. doi: 10.1128/mcb.2.4.386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Alt F. W., Yancopoulos G. D., Blackwell T. K., Wood C., Thomas E., Boss M., Coffman R., Rosenberg N., Tonegawa S., Baltimore D. Ordered rearrangement of immunoglobulin heavy chain variable region segments. EMBO J. 1984 Jun;3(6):1209–1219. doi: 10.1002/j.1460-2075.1984.tb01955.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Atchison M. L., Perry R. P. The role of the kappa enhancer and its binding factor NF-kappa B in the developmental regulation of kappa gene transcription. Cell. 1987 Jan 16;48(1):121–128. doi: 10.1016/0092-8674(87)90362-x. [DOI] [PubMed] [Google Scholar]
  7. Bain G., Maandag E. C., Izon D. J., Amsen D., Kruisbeek A. M., Weintraub B. C., Krop I., Schlissel M. S., Feeney A. J., van Roon M. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell. 1994 Dec 2;79(5):885–892. doi: 10.1016/0092-8674(94)90077-9. [DOI] [PubMed] [Google Scholar]
  8. Barberis A., Widenhorn K., Vitelli L., Busslinger M. A novel B-cell lineage-specific transcription factor present at early but not late stages of differentiation. Genes Dev. 1990 May;4(5):849–859. doi: 10.1101/gad.4.5.849. [DOI] [PubMed] [Google Scholar]
  9. Betz A. G., Milstein C., González-Fernández A., Pannell R., Larson T., Neuberger M. S. Elements regulating somatic hypermutation of an immunoglobulin kappa gene: critical role for the intron enhancer/matrix attachment region. Cell. 1994 Apr 22;77(2):239–248. doi: 10.1016/0092-8674(94)90316-6. [DOI] [PubMed] [Google Scholar]
  10. Blasquez V. C., Hale M. A., Trevorrow K. W., Garrard W. T. Immunoglobulin kappa gene enhancers synergistically activate gene expression but independently determine chromatin structure. J Biol Chem. 1992 Nov 25;267(33):23888–23893. [PubMed] [Google Scholar]
  11. Blasquez V. C., Xu M., Moses S. C., Garrard W. T. Immunoglobulin kappa gene expression after stable integration. I. Role of the intronic MAR and enhancer in plasmacytoma cells. J Biol Chem. 1989 Dec 15;264(35):21183–21189. [PubMed] [Google Scholar]
  12. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  13. Brooks K., Yuan D., Uhr J. W., Krammer P. H., Vitetta E. S. Lymphokine-induced IgM secretion by clones of neoplastic B cells. Nature. 1983 Apr 28;302(5911):825–826. doi: 10.1038/302825a0. [DOI] [PubMed] [Google Scholar]
  14. Chen-Bettecken U., Wecker E., Schimpl A. Transcriptional control of mu- and kappa-gene expression in resting and bacterial lipopolysaccharide-activated normal B cells. Immunobiology. 1987 Mar;174(2):162–176. doi: 10.1016/s0171-2985(87)80036-0. [DOI] [PubMed] [Google Scholar]
  15. Contreras R., Fiers W. Initiation of transcription by RNA polymerase II in permeable, SV40-infected or noninfected, CVI cells; evidence for multiple promoters of SV40 late transcription. Nucleic Acids Res. 1981 Jan 24;9(2):215–236. doi: 10.1093/nar/9.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Czerny T., Schaffner G., Busslinger M. DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site. Genes Dev. 1993 Oct;7(10):2048–2061. doi: 10.1101/gad.7.10.2048. [DOI] [PubMed] [Google Scholar]
  17. Dariavach P., Williams G. T., Campbell K., Pettersson S., Neuberger M. S. The mouse IgH 3'-enhancer. Eur J Immunol. 1991 Jun;21(6):1499–1504. doi: 10.1002/eji.1830210625. [DOI] [PubMed] [Google Scholar]
  18. Davidson W. F., Pierce J. H., Rudikoff S., Morse H. C., 3rd Relationships between B cell and myeloid differentiation. Studies with a B lymphocyte progenitor line, HAFTL-1. J Exp Med. 1988 Jul 1;168(1):389–407. doi: 10.1084/jem.168.1.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Faisst S., Meyer S. Compilation of vertebrate-encoded transcription factors. Nucleic Acids Res. 1992 Jan 11;20(1):3–26. doi: 10.1093/nar/20.1.3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fulton R., Van Ness B. Kappa immunoglobulin promoters and enhancers display developmentally controlled interactions. Nucleic Acids Res. 1993 Oct 25;21(21):4941–4947. doi: 10.1093/nar/21.21.4941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Giese K., Cox J., Grosschedl R. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell. 1992 Apr 3;69(1):185–195. doi: 10.1016/0092-8674(92)90129-z. [DOI] [PubMed] [Google Scholar]
  23. Goodhardt M., Babinet C., Lutfalla G., Kallenbach S., Cavelier P., Rougeon F. Immunoglobulin kappa light chain gene promoter and enhancer are not responsible for B-cell restricted gene rearrangement. Nucleic Acids Res. 1989 Sep 25;17(18):7403–7415. doi: 10.1093/nar/17.18.7403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gross D. S., Garrard W. T. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159–197. doi: 10.1146/annurev.bi.57.070188.001111. [DOI] [PubMed] [Google Scholar]
  25. Haggerty H. G., Wechsler R. J., Lentz V. M., Monroe J. G. Endogenous expression of delta on the surface of WEHI-231. Characterization of its expression and signaling properties. J Immunol. 1993 Nov 1;151(9):4681–4693. [PubMed] [Google Scholar]
  26. Hardy R. R., Carmack C. E., Shinton S. A., Kemp J. D., Hayakawa K. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med. 1991 May 1;173(5):1213–1225. doi: 10.1084/jem.173.5.1213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hariharan N., Kelley D. E., Perry R. P. Delta, a transcription factor that binds to downstream elements in several polymerase II promoters, is a functionally versatile zinc finger protein. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9799–9803. doi: 10.1073/pnas.88.21.9799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hiramatsu R., Akagi K., Matsuoka M., Sakumi K., Nakamura H., Kingsbury L., David C., Hardy R. R., Yamamura K., Sakano H. The 3' enhancer region determines the B/T specificity and pro-B/pre-B specificity of immunoglobulin V kappa-J kappa joining. Cell. 1995 Dec 29;83(7):1113–1123. doi: 10.1016/0092-8674(95)90138-8. [DOI] [PubMed] [Google Scholar]
  29. Holmes K. L., Pierce J. H., Davidson W. F., Morse H. C., 3rd Murine hematopoietic cells with pre-B or pre-B/myeloid characteristics are generated by in vitro transformation with retroviruses containing fes, ras, abl, and src oncogenes. J Exp Med. 1986 Aug 1;164(2):443–457. doi: 10.1084/jem.164.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Judde J. G., Max E. E. Characterization of the human immunoglobulin kappa gene 3' enhancer: functional importance of three motifs that demonstrate B-cell-specific in vivo footprints. Mol Cell Biol. 1992 Nov;12(11):5206–5216. doi: 10.1128/mcb.12.11.5206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Keene M. A., Elgin S. C. Micrococcal nuclease as a probe of DNA sequence organization and chromatin structure. Cell. 1981 Nov;27(1 Pt 2):57–64. doi: 10.1016/0092-8674(81)90360-3. [DOI] [PubMed] [Google Scholar]
  32. Kelley D. E., Perry R. P. Transcriptional and posttranscriptional control of immunoglobulin mRNA production during B lymphocyte development. Nucleic Acids Res. 1986 Jul 11;14(13):5431–5447. doi: 10.1093/nar/14.13.5431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kozmik Z., Wang S., Dörfler P., Adams B., Busslinger M. The promoter of the CD19 gene is a target for the B-cell-specific transcription factor BSAP. Mol Cell Biol. 1992 Jun;12(6):2662–2672. doi: 10.1128/mcb.12.6.2662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lenardo M., Pierce J. W., Baltimore D. Protein-binding sites in Ig gene enhancers determine transcriptional activity and inducibility. Science. 1987 Jun 19;236(4808):1573–1577. doi: 10.1126/science.3109035. [DOI] [PubMed] [Google Scholar]
  35. Liao F., Giannini S. L., Birshtein B. K. A nuclear DNA-binding protein expressed during early stages of B cell differentiation interacts with diverse segments within and 3' of the Ig H chain gene cluster. J Immunol. 1992 May 1;148(9):2909–2917. [PubMed] [Google Scholar]
  36. Liou H. C., Sha W. C., Scott M. L., Baltimore D. Sequential induction of NF-kappa B/Rel family proteins during B-cell terminal differentiation. Mol Cell Biol. 1994 Aug;14(8):5349–5359. doi: 10.1128/mcb.14.8.5349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. McGhee J. D., Felsenfeld G. Reaction of nucleosome DNA with dimethyl sulfate. Proc Natl Acad Sci U S A. 1979 May;76(5):2133–2137. doi: 10.1073/pnas.76.5.2133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. McPherson C. E., Shim E. Y., Friedman D. S., Zaret K. S. An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell. 1993 Oct 22;75(2):387–398. doi: 10.1016/0092-8674(93)80079-t. [DOI] [PubMed] [Google Scholar]
  39. Meyer K. B., Ireland J. Activation of the immunoglobulin kappa 3' enhancer in pre-B cells correlates with the suppression of a nuclear factor binding to a sequence flanking the active core. Nucleic Acids Res. 1994 May 11;22(9):1576–1582. doi: 10.1093/nar/22.9.1576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Meyer K. B., Neuberger M. S. The immunoglobulin kappa locus contains a second, stronger B-cell-specific enhancer which is located downstream of the constant region. EMBO J. 1989 Jul;8(7):1959–1964. doi: 10.1002/j.1460-2075.1989.tb03601.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Meyer K. B., Sharpe M. J., Surani M. A., Neuberger M. S. The importance of the 3'-enhancer region in immunoglobulin kappa gene expression. Nucleic Acids Res. 1990 Oct 11;18(19):5609–5615. doi: 10.1093/nar/18.19.5609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Miyamoto S., Schmitt M. J., Verma I. M. Qualitative changes in the subunit composition of kappa B-binding complexes during murine B-cell differentiation. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5056–5060. doi: 10.1073/pnas.91.11.5056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Mueller P. R., Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
  44. Murre C., McCaw P. S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 1989 Mar 10;56(5):777–783. doi: 10.1016/0092-8674(89)90682-x. [DOI] [PubMed] [Google Scholar]
  45. Murre C., McCaw P. S., Vaessin H., Caudy M., Jan L. Y., Jan Y. N., Cabrera C. V., Buskin J. N., Hauschka S. D., Lassar A. B. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell. 1989 Aug 11;58(3):537–544. doi: 10.1016/0092-8674(89)90434-0. [DOI] [PubMed] [Google Scholar]
  46. Murre C., Voronova A., Baltimore D. B-cell- and myocyte-specific E2-box-binding factors contain E12/E47-like subunits. Mol Cell Biol. 1991 Feb;11(2):1156–1160. doi: 10.1128/mcb.11.2.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Mushinski J. F., Davidson W. F., Morse H. C., 3rd Activation of cellular oncogenes in human and mouse leukemia-lymphomas: spontaneous and induced oncogene expression in murine B lymphocytic neoplasms. Cancer Invest. 1987;5(4):345–368. [PubMed] [Google Scholar]
  48. Neurath M. F., Max E. E., Strober W. Pax5 (BSAP) regulates the murine immunoglobulin 3' alpha enhancer by suppressing binding of NF-alpha P, a protein that controls heavy chain transcription. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5336–5340. doi: 10.1073/pnas.92.12.5336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Neurath M. F., Strober W., Wakatsuki Y. The murine Ig 3' alpha enhancer is a target site with repressor function for the B cell lineage-specific transcription factor BSAP (NF-HB, S alpha-BP). J Immunol. 1994 Jul 15;153(2):730–742. [PubMed] [Google Scholar]
  50. Okabe T., Watanabe T., Kudo A. A pre-B- and B cell-specific DNA-binding protein, EBB-1, which binds to the promoter of the VpreB1 gene. Eur J Immunol. 1992 Jan;22(1):37–43. doi: 10.1002/eji.1830220107. [DOI] [PubMed] [Google Scholar]
  51. Palacios R., Karasuyama H., Rolink A. Ly1+ PRO-B lymphocyte clones. Phenotype, growth requirements and differentiation in vitro and in vivo. EMBO J. 1987 Dec 1;6(12):3687–3693. doi: 10.1002/j.1460-2075.1987.tb02702.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Park K., Atchison M. L. Isolation of a candidate repressor/activator, NF-E1 (YY-1, delta), that binds to the immunoglobulin kappa 3' enhancer and the immunoglobulin heavy-chain mu E1 site. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9804–9808. doi: 10.1073/pnas.88.21.9804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pfeifer G. P., Riggs A. D. Chromatin differences between active and inactive X chromosomes revealed by genomic footprinting of permeabilized cells using DNase I and ligation-mediated PCR. Genes Dev. 1991 Jun;5(6):1102–1113. doi: 10.1101/gad.5.6.1102. [DOI] [PubMed] [Google Scholar]
  54. Pfeifer G. P., Tanguay R. L., Steigerwald S. D., Riggs A. D. In vivo footprint and methylation analysis by PCR-aided genomic sequencing: comparison of active and inactive X chromosomal DNA at the CpG island and promoter of human PGK-1. Genes Dev. 1990 Aug;4(8):1277–1287. doi: 10.1101/gad.4.8.1277. [DOI] [PubMed] [Google Scholar]
  55. Picard D., Schaffner W. A lymphocyte-specific enhancer in the mouse immunoglobulin kappa gene. Nature. 1984 Jan 5;307(5946):80–82. doi: 10.1038/307080a0. [DOI] [PubMed] [Google Scholar]
  56. Pongubala J. M., Atchison M. L. Activating transcription factor 1 and cyclic AMP response element modulator can modulate the activity of the immunoglobulin kappa 3' enhancer. J Biol Chem. 1995 Apr 28;270(17):10304–10313. doi: 10.1074/jbc.270.17.10304. [DOI] [PubMed] [Google Scholar]
  57. Pongubala J. M., Atchison M. L. Functional characterization of the developmentally controlled immunoglobulin kappa 3' enhancer: regulation by Id, a repressor of helix-loop-helix transcription factors. Mol Cell Biol. 1991 Feb;11(2):1040–1047. doi: 10.1128/mcb.11.2.1040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Pongubala J. M., Nagulapalli S., Klemsz M. J., McKercher S. R., Maki R. A., Atchison M. L. PU.1 recruits a second nuclear factor to a site important for immunoglobulin kappa 3' enhancer activity. Mol Cell Biol. 1992 Jan;12(1):368–378. doi: 10.1128/mcb.12.1.368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Queen C., Baltimore D. Immunoglobulin gene transcription is activated by downstream sequence elements. Cell. 1983 Jul;33(3):741–748. doi: 10.1016/0092-8674(83)90016-8. [DOI] [PubMed] [Google Scholar]
  60. Reed K. C., Mann D. A. Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res. 1985 Oct 25;13(20):7207–7221. doi: 10.1093/nar/13.20.7207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Reth M. G., Ammirati P., Jackson S., Alt F. W. Regulated progression of a cultured pre-B-cell line to the B-cell stage. 1985 Sep 26-Oct 2Nature. 317(6035):353–355. doi: 10.1038/317353a0. [DOI] [PubMed] [Google Scholar]
  62. Rolink A., Melchers F. Molecular and cellular origins of B lymphocyte diversity. Cell. 1991 Sep 20;66(6):1081–1094. doi: 10.1016/0092-8674(91)90032-t. [DOI] [PubMed] [Google Scholar]
  63. Schlissel M. S., Baltimore D. Activation of immunoglobulin kappa gene rearrangement correlates with induction of germline kappa gene transcription. Cell. 1989 Sep 8;58(5):1001–1007. doi: 10.1016/0092-8674(89)90951-3. [DOI] [PubMed] [Google Scholar]
  64. Sha W. C., Liou H. C., Tuomanen E. I., Baltimore D. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell. 1995 Jan 27;80(2):321–330. doi: 10.1016/0092-8674(95)90415-8. [DOI] [PubMed] [Google Scholar]
  65. Singh M., Birshtein B. K. NF-HB (BSAP) is a repressor of the murine immunoglobulin heavy-chain 3' alpha enhancer at early stages of B-cell differentiation. Mol Cell Biol. 1993 Jun;13(6):3611–3622. doi: 10.1128/mcb.13.6.3611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Staudt L. M., Lenardo M. J. Immunoglobulin gene transcription. Annu Rev Immunol. 1991;9:373–398. doi: 10.1146/annurev.iy.09.040191.002105. [DOI] [PubMed] [Google Scholar]
  67. Sun X. H. Constitutive expression of the Id1 gene impairs mouse B cell development. Cell. 1994 Dec 2;79(5):893–900. doi: 10.1016/0092-8674(94)90078-7. [DOI] [PubMed] [Google Scholar]
  68. Takeda S., Zou Y. R., Bluethmann H., Kitamura D., Muller U., Rajewsky K. Deletion of the immunoglobulin kappa chain intron enhancer abolishes kappa chain gene rearrangement in cis but not lambda chain gene rearrangement in trans. EMBO J. 1993 Jun;12(6):2329–2336. doi: 10.1002/j.1460-2075.1993.tb05887.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Travis A., Amsterdam A., Belanger C., Grosschedl R. LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor alpha enhancer function [corrected]. Genes Dev. 1991 May;5(5):880–894. doi: 10.1101/gad.5.5.880. [DOI] [PubMed] [Google Scholar]
  70. Van Ness B. G., Weigert M., Coleclough C., Mather E. L., Kelley D. E., Perry R. P. Transcription of the unrearranged mouse C kappa locus: sequence of the initiation region and comparison of activity with a rearranged V kappa-C kappa gene. Cell. 1981 Dec;27(3 Pt 2):593–602. doi: 10.1016/0092-8674(81)90401-3. [DOI] [PubMed] [Google Scholar]
  71. Wallrath L. L., Lu Q., Granok H., Elgin S. C. Architectural variations of inducible eukaryotic promoters: preset and remodeling chromatin structures. Bioessays. 1994 Mar;16(3):165–170. doi: 10.1002/bies.950160306. [DOI] [PubMed] [Google Scholar]
  72. Weih F., Carrasco D., Durham S. K., Barton D. S., Rizzo C. A., Ryseck R. P., Lira S. A., Bravo R. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-kappa B/Rel family. Cell. 1995 Jan 27;80(2):331–340. doi: 10.1016/0092-8674(95)90416-6. [DOI] [PubMed] [Google Scholar]
  73. Wilson R. B., Kiledjian M., Shen C. P., Benezra R., Zwollo P., Dymecki S. M., Desiderio S. V., Kadesch T. Repression of immunoglobulin enhancers by the helix-loop-helix protein Id: implications for B-lymphoid-cell development. Mol Cell Biol. 1991 Dec;11(12):6185–6191. doi: 10.1128/mcb.11.12.6185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980 Aug 28;286(5776):854–860. doi: 10.1038/286854a0. [DOI] [PubMed] [Google Scholar]
  75. Yancopoulos G. D., Alt F. W. Developmentally controlled and tissue-specific expression of unrearranged VH gene segments. Cell. 1985 Feb;40(2):271–281. doi: 10.1016/0092-8674(85)90141-2. [DOI] [PubMed] [Google Scholar]
  76. Yuan D., Tucker P. W. Transcriptional regulation of the mu-delta heavy chain locus in normal murine B lymphocytes. J Exp Med. 1984 Aug 1;160(2):564–583. doi: 10.1084/jem.160.2.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Zhang L., Gralla J. D. In situ nucleoprotein structure at the SV40 major late promoter: melted and wrapped DNA flank the start site. Genes Dev. 1989 Nov;3(11):1814–1822. doi: 10.1101/gad.3.11.1814. [DOI] [PubMed] [Google Scholar]
  78. Zhuang Y., Soriano P., Weintraub H. The helix-loop-helix gene E2A is required for B cell formation. Cell. 1994 Dec 2;79(5):875–884. doi: 10.1016/0092-8674(94)90076-0. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES